Intestinal Ralstonia pickettii augments glucose intolerance in obesity

An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus (T2DM). Low grade inflammation, potentially initiated by the intestinal microbiota, has been suggested to be a driving force in the development of...

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Published inPloS one Vol. 12; no. 11; p. e0181693
Main Authors Udayappan, Shanthadevi D., Kovatcheva-Datchary, Petia, Bakker, Guido J., Havik, Stefan R., Herrema, Hilde, Cani, Patrice D., Bouter, Kristien E., Belzer, Clara, Witjes, Julia J., Vrieze, Anne, de Sonnaville, Noor, Chaplin, Alice, van Raalte, Daniel H., Aalvink, Steven, Dallinga-Thie, Geesje M., Heilig, Hans G. H. J., Bergström, Göran, van der Meij, Suzan, van Wagensveld, Bart A., Hoekstra, Joost B. L., Holleman, Frits, Stroes, Erik S. G., Groen, Albert K., Bäckhed, Fredrik, de Vos, Willem M., Nieuwdorp, Max
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 22.11.2017
Public Library of Science (PLoS)
Subjects
Adipose tissue
Bacteria
Biology and Life Sciences
Deoxyribonucleic acid
Development and progression
Diabetes
Diabetes mellitus
diet-induced obesity
DNA
Endocrinology and Diabetes
Endokrinologi och diabetes
Endotoxins
fat
gastrointestinal-tract
Glucose
Glucose intolerance
Glucose tolerance
gut microbiota
immunity
Insulin
Insulin resistance
Intestinal microflora
Intestine
Intolerance
Laboratorium voor Microbiologie
low-grade inflammation
Medicine and Health Sciences
Metabolic diseases
Metabolic disorders
metabolic syndrome
Mice
Microbiological Laboratory
Microbiologie
Microbiology
Microbiota
Microbiota (Symbiotic organisms)
Obesity
Pathogenesis
Physical sciences
Physiological aspects
Ralstonia pickettii
receptor 5
Risk factors
Rodents
rRNA 16S
Soil bacteria
Teaching hospitals
VLAG
WIMEK
Netherlands
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0181693

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Abstract An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus (T2DM). Low grade inflammation, potentially initiated by the intestinal microbiota, has been suggested to be a driving force in the development of insulin resistance in obesity. Here, we report that bacterial DNA is present in mesenteric adipose tissue of obese but otherwise healthy human subjects. Pyrosequencing of bacterial 16S rRNA genes revealed that DNA from the Gram-negative species Ralstonia was most prevalent. Interestingly, fecal abundance of Ralstonia pickettii was increased in obese subjects with pre-diabetes and T2DM. To assess if R. pickettii was causally involved in development of obesity and T2DM, we performed a proof-of-concept study in diet-induced obese (DIO) mice. Compared to vehicle-treated control mice, R. pickettii-treated DIO mice had reduced glucose tolerance. In addition, circulating levels of endotoxin were increased in R. pickettii-treated mice. In conclusion, this study suggests that intestinal Ralstonia is increased in obese human subjects with T2DM and reciprocally worsens glucose tolerance in DIO mice.
AbstractList An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus (T2DM). Low grade inflammation, potentially initiated by the intestinal microbiota, has been suggested to be a driving force in the development of insulin resistance in obesity. Here, we report that bacterial DNA is present in mesenteric adipose tissue of obese but otherwise healthy human subjects. Pyrosequencing of bacterial 16S rRNA genes revealed that DNA from the Gram-negative species Ralstonia was most prevalent. Interestingly, fecal abundance of Ralstonia pickettii was increased in obese subjects with pre-diabetes and T2DM. To assess if R. pickettii was causally involved in development of obesity and T2DM, we performed a proof-of-concept study in diet-induced obese (DIO) mice. Compared to vehicle-treated control mice, R. pickettii-treated DIO mice had reduced glucose tolerance. In addition, circulating levels of endotoxin were increased in R. pickettii-treated mice. In conclusion, this study suggests that intestinal Ralstonia is increased in obese human subjects with T2DM and reciprocally worsens glucose tolerance in DIO mice.
An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus (T2DM). Low grade inflammation, potentially initiated by the intestinal microbiota, has been suggested to be a driving force in the development of insulin resistance in obesity. Here, we report that bacterial DNA is present in mesenteric adipose tissue of obese but otherwise healthy human subjects. Pyrosequencing of bacterial 16S rRNA genes revealed that DNA from the Gram-negative species Ralstonia was most prevalent. Interestingly, fecal abundance of Ralstonia pickettii was increased in obese subjects with pre-diabetes and T2DM. To assess if R. pickettii was causally involved in development of obesity and T2DM, we performed a proof-of-concept study in diet-induced obese (DIO) mice. Compared to vehicle-treated control mice, R. pickettii-treated DIO mice had reduced glucose tolerance. In addition, circulating levels of endotoxin were increased in R. pickettii-treated mice. In conclusion, this study suggests that intestinal Ralstonia is increased in obese human subjects with T2DM and reciprocally worsens glucose tolerance in DIO mice.An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus (T2DM). Low grade inflammation, potentially initiated by the intestinal microbiota, has been suggested to be a driving force in the development of insulin resistance in obesity. Here, we report that bacterial DNA is present in mesenteric adipose tissue of obese but otherwise healthy human subjects. Pyrosequencing of bacterial 16S rRNA genes revealed that DNA from the Gram-negative species Ralstonia was most prevalent. Interestingly, fecal abundance of Ralstonia pickettii was increased in obese subjects with pre-diabetes and T2DM. To assess if R. pickettii was causally involved in development of obesity and T2DM, we performed a proof-of-concept study in diet-induced obese (DIO) mice. Compared to vehicle-treated control mice, R. pickettii-treated DIO mice had reduced glucose tolerance. In addition, circulating levels of endotoxin were increased in R. pickettii-treated mice. In conclusion, this study suggests that intestinal Ralstonia is increased in obese human subjects with T2DM and reciprocally worsens glucose tolerance in DIO mice.
Audience Academic
Author Dallinga-Thie, Geesje M.
Holleman, Frits
Chaplin, Alice
Bouter, Kristien E.
Stroes, Erik S. G.
Bäckhed, Fredrik
Nieuwdorp, Max
Witjes, Julia J.
Bergström, Göran
Vrieze, Anne
Havik, Stefan R.
van Raalte, Daniel H.
Bakker, Guido J.
van Wagensveld, Bart A.
de Vos, Willem M.
Aalvink, Steven
Udayappan, Shanthadevi D.
Cani, Patrice D.
de Sonnaville, Noor
Kovatcheva-Datchary, Petia
Herrema, Hilde
Belzer, Clara
Groen, Albert K.
Heilig, Hans G. H. J.
van der Meij, Suzan
Hoekstra, Joost B. L.
AuthorAffiliation Technische Universitat Dresden, GERMANY
6 Diabetes Center, Department of Internal medicine, VU University Medical Center, Amsterdam, The Netherlands
10 Department of Pediatrics, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
11 Novo Nordisk Foundation Center for Basic Metabolic Research, Section for Metabolic Receptology and Enteroendocrinology, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark
2 Wallenberg Laboratory, University of Gothenburg, Sahlgrenska University Hospital, Gothenburg, Sweden
4 Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands
1 Department of Vascular Medicine, Academic Medical Center, Amsterdam, The Netherlands
12 RPU Immunobiology, University of Helsinki, Helsinki, Finland
8 Department of Surgery, Flevo Hospital, Almere, The Netherlands
7 ICAR, VU University Medical Center, Amsterdam, The Netherlands
3 Université catholique de Louvain, WELBIO (Walloon Excellence in Life sciences a
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29166392$$D View this record in MEDLINE/PubMed
https://gup.ub.gu.se/publication/261477$$DView record from Swedish Publication Index
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Udayappan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2017 Udayappan et al 2017 Udayappan et al
Wageningen University & Research
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– notice: 2017 Udayappan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2017 Udayappan et al 2017 Udayappan et al
– notice: Wageningen University & Research
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Competing Interests: We have the following interests. This study was partly funded by AFA insurances. M.N. and W.M.deV. are founders, own equity and are in the Scientific Advisory Board of Caelus Pharmaceuticals, the Netherlands; WMdV is in the Scientific Advisory Board of Chr Hansen Horsholm Danmark and the M.N. and W.M.deV. are founders, own equity and are in the Scientific Advisory Board of Caelus Pharmaceutical(NIHS) Lausanne Switzerland. F.B. is a founder of MetaboGen AB, Sweden. F.B. and G.B own equity in MetaboGen AB, Sweden. None of these are directly relevant to the current paper. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.
ORCID 0000-0002-0112-6348
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Snippet An altered intestinal microbiota composition has been implicated in the pathogenesis of metabolic disease including obesity and type 2 diabetes mellitus...
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SubjectTerms Adipose tissue
Bacteria
Biology and Life Sciences
Deoxyribonucleic acid
Development and progression
Diabetes
Diabetes mellitus
diet-induced obesity
DNA
Endocrinology and Diabetes
Endokrinologi och diabetes
Endotoxins
fat
gastrointestinal-tract
Glucose
Glucose intolerance
Glucose tolerance
gut microbiota
immunity
Insulin
Insulin resistance
Intestinal microflora
Intestine
Intolerance
Laboratorium voor Microbiologie
low-grade inflammation
Medicine and Health Sciences
Metabolic diseases
Metabolic disorders
metabolic syndrome
Mice
Microbiological Laboratory
Microbiologie
Microbiology
Microbiota
Microbiota (Symbiotic organisms)
Obesity
Pathogenesis
Physical sciences
Physiological aspects
Ralstonia pickettii
receptor 5
Risk factors
Rodents
rRNA 16S
Soil bacteria
Teaching hospitals
VLAG
WIMEK
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Title Intestinal Ralstonia pickettii augments glucose intolerance in obesity
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